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An Overview of the Hydraulic Systems in Early Land Plants

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An Overview of the Hydraulic Systems in Early Land Plants Strullu-DerrienIAWA et Journal al. – Hydraulic 34 (4), 2013:systems 333–351 in early land plants 333 AN OVERVIEW OF THE HYDRaULIC SYSTEMS IN EaRLY LaND PLaNTS Christine Strullu-Derrien1,*, Paul Kenrick1, Eric Badel2,3, Hervé Cochard2,3 and Paul Tafforeau4 1Department of Earth Sciences, The Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom 2INRA, UMR547 PIAF, 63100 Clermont-Ferrand, France 3Clermont Université, Université Blaise Pascal, UMR547 PIAF, 63000 Clermont-Ferrand, France 4European Synchrotron Radiation Facility, 6 rue Jules Horowitz, 38043 Grenoble cedex, France *Corresponding author; e-mail: [email protected] abstract One of the key functions of wood is hydraulic conductivity, and the general physical properties controlling this are well characterized in living plants. Modern species capture only a fraction of the known diversity of wood, which is well preserved in a fossil record that extends back over 400 million years to the origin of the vascular plants. Early fossil woods are known to differ in many key respects from woods of modern gymnosperms (e.g., tracheid size, secondary wall thickenings, lignin chemistry, cambium development) and recent discoveries are shedding new light on the earliest stages of wood evolution, rais- ing questions about the performance of these systems and their functions. We provide an overview of the early fossil record focusing on tracheid morphology in the earliest primary and secondary xylem and on cambial development. The fossil record clearly shows that wood evolved in small stature plants prior to the evolution of a distinctive leaf-stem-root organography. The hydraulic proper- ties of fossil woods cannot be measured directly, but with the development of mathematical models it is becoming increasingly feasible to make inferences and quantify performance, enabling comparison with modern woods. Perhaps the most difficult aspect of hydraulic conductance to quantify is the resistance of pits and other highly distinctive and unique secondary wall features in the earliest tracheids. New analytical methods, in particular X-ray synchrotron microtomography (PPC-SRμCT), open up the possibility of creating dynamic, three-dimensional models of permineralized woods facilitating the analysis of hydraulic and biomechanical properties. Keywords: Wood, fossil, synchrotron, 3D model, permineralization, hydraulic properties. Introduction The evolution of the vascular system in plants was a key development in the history of life because of its fundamental role in water transport and, in many species, its ancillary function as a framework of structural support (Sperry 2003; Pittermann 2010; Lucas © International Association of Wood Anatomists, 2013 DOI 10.1163/22941932-00000029 Published by Koninklijke Brill NV, Leiden Downloaded from Brill.com10/09/2021 05:09:00PM via free access 334 IAWA Journal 34 (4), 2013 Monilophytes Lignophytes Bryophytes Lycophytes Euphyllophytes 299 Pen Car Mis 359 Filicophytes U Charales Spermatophytes Sphenophytes Lycopsids Archaeopteridales Dev M Aneurophytales Cladoxylopsids Marchiantiophytes Rhyniophytes Psilophyton L Bryophytes Zosterophyllopsids 416 Cooksonia Sil Anthocerophytes Tracheophytes 443 Coleochaetales Ord Embryophytes 488 C-Type tracheids S-Type tracheids G-Type tracheids P-Type tracheids Secondary xylem, unifacial cambium Secondary xylem, bifacial cambium Figure 1. Simplified phylogenetic tree showing the minimum stratigraphic ranges of selected groups based on megafossils (bars) and their minimum implied range extensions (lines). Tracheid and secondary xylem types are shown on the figure. Ord = Ordovician; Sil = Silurian; Dev = Devonian, L = Lower, M = Middle, U = Upper; Car = Carboniferous. Mis = Mississippian, Pen = Pennsylvanian. Adapted from Kenrick & Crane (1997b). et al. 2013). The vascular plants or tracheophytes are defined by the possession of this tissue system, the acquisition of which was essential to the evolution of their diverse forms, leading ultimately to their dominance of terrestrial ecosystems (Niklas 1997; Bateman et al. 1998; Labandeira 2005). The main constituents of the vascular system are phloem and xylem, but it is the latter that is more commonly encountered in the fossil record due to the resilience of its cellular components, which typically possess robust cell walls containing the polyphenolic polymer lignin (Boyce et al. 2004). Vascular tissues first appear in the fossil record in the lower part of the Devonian Period (410– 407 Myr) (Fig. 1) when terrestrial sediments containing fossil plants first became abundant (Gensel 2008; Kenrick et al. 2012). Research over the past 25 years has revealed some of the earliest stages in the evolution of the xylem (Stein 1993) and in particular has focused on the interpretation and documentation of its main component, the tracheid (Kenrick & Crane 1991; Edwards 1993; Friedman & Cook 2000; Sperry 2003). Several distinctive types of tracheid are now widely recognized, providing de- tailed information on the structure of the cell wall and insights into the early evolution of this important cell type. The vascular system in the earliest tracheophytes was entirely primary, but the fossil record has also provided much information on the evolution of secondary vascular tissue (Cichan 1986; Cichan & Taylor 1990; Meyer-Berthaud et al. 2010; Spicer & Groover 2010; Gerrienne et al. 2011). Cambial activity in plants initially evolved indepen- Downloaded from Brill.com10/09/2021 05:09:00PM via free access Strullu-Derrien et al. – Hydraulic systems in early land plants 335 dently at least twice in the Devonian Period (Kenrick & Crane 1997a, b) and perhaps on more occasions (Boyce 2010) (Fig. 1). In many extinct groups the cambium was unifacial, developing only secondary xylem, and it was unable to undergo anticlinal cell division (Taylor et al. 2009; Spicer & Groover 2010). This type of cambium pro- duced the secondary xylem in the extinct tree cladoxylopsids of the Devonian Period and the lycopods and horsetails of the Carboniferous Period (Niklas 1997; Stein et al. 2007; Meyer-Berthaud et al. 2010). These trees generally produced rather little wood, and the vascular cylinder had limited capacity to increase in volume while maintain- ing the integrity of the cambium (Cichan 1986). The more familiar bifacial cambium gives rise to both secondary xylem and secondary phloem, and it has the capacity to undergo anticlinal cell division (Donoghue 2005). This form of cambium evolved during the Devonian Period in the lineage leading to gymnosperms and angiosperms (Hilton & Bateman 2006). New information from the early fossil record is providing further tantalizing insights that are promising to unravel the sequence of acquisition of characteristics that led to the evolution of secondary xylem (Gerrienne et al. 2011). Our growing knowledge of the early evolution of vascular tissues derived from the careful study of fossils raises questions about the performance of these systems and their functional roles in the early development of vascular plants. Recent advances in our understanding of the hydraulics of modern woods (Hacke et al. 2004; Pittermann et al. 2006; Pittermann 2010) and the development and application of mathematical methods to infer the hydraulic properties of fossil woods (Wilson et al. 2008; Wilson & Knoll 2010; Wilson & Fischer 2011) mean that we now have many of the tools that we need to begin to investigate the hydraulic characteristics of the earliest vascular systems in plants. Early fossil wood is typically permineralized, and various methods that have been developed to investigate and characterize its structure include the preparation of sections for light microscopy and scanning electron microscopy (Jones & Rowe 1999). These are invasive, and they are frequently also destructive. The development of X-ray computed tomography, in particular the use of high-resolution tools such as synchrotrons, provides an efficient non-destructive alternative (e.g., Friis et al. 2007). Here we give a succinct overview of the earliest fossil record of primary and secondary xylem and its cellular components and an introduction to recent research on its hydraulic properties. We show how synchrotron microtomography can be used to investigate the hydraulic properties of the earliest wood. The earliest fossil evidence of vascular elements and their hYdraulic structures Xylem and tracheid cell structure are frequently well preserved in the fossil record enabling both biomechanical properties and hydraulic efficiency to be estimated, further- ing our understanding of the functional evolution of wood (Niklas 1997; Sperry 2003; Pittermann 2010). In fossils of the early part of the Devonian period the vascular system typically is permineralized in a variety of minerals including pyrite and its oxidation products (Kenrick 1999) (Fig. 2c–e), more rarely silicates (Channing & Edwards 2009), calcium/magnesium carbonates (Hartman & Banks 1980), or is simply preserved as Downloaded from Brill.com10/09/2021 05:09:00PM via free access 336 IAWA Journal 34 (4), 2013 b Figure 2. – a: Cooksonia pertoni: the earliest tracheophyte (Herefordshire, England; specimen nr. V58010 Lang collection, Natural History Museum, London). Scale bar = 0.15 mm. – b: Coali- fied tracheid in Cooksonia pertoni (C-type tracheid). Note the thick coalified wall and mineral infill of lumen with grooves marking positions of secondary thickenings (From Edwards, New Phytologist, 1993; with courtesy). Scale bar = 0.8 μm.
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